Hepatocyte growth factor exerts its anti-inflammatory action by disrupting nuclear factor-kappaB signaling

Am J Pathol. 2008 Jul;173(1):30-41. doi: 10.2353/ajpath.2008.070583. Epub 2008 May 23.

Abstract

Renal inflammation, characterized by the influx of inflammatory cells, is believed to play a critical role in the initiation and progression of a wide range of chronic kidney diseases. Here, we show that hepatocyte growth factor (HGF) inhibited renal inflammation and proinflammatory chemokine expression by disrupting nuclear factor (NF)-kappaB signaling. In vivo, HGF gene delivery inhibited interstitial infiltration of inflammatory T cells and macrophages, and suppressed expression of both RANTES (regulated on activation, normal T cell expressed and secreted) and monocyte chemoattractant protein-1 in a mouse model of obstructive nephropathy. In vitro, HGF abolished RANTES induction in human kidney epithelial cells, which was dependent on NF-kappaB signaling. HGF did not significantly affect the phosphorylation or degradation of IkappaBalpha; it also did not influence the phosphorylation or nuclear translocation of p65 NF-kappaB. However, HGF prevented p65 NF-kappaB binding to its cognate cis-acting element in the RANTES promoter. HGF action was dependent on the activation of the phosphoinositide 3-kinase/Akt pathway, which led to the phosphorylation and inactivation of glycogen synthase kinase (GSK)-3beta. Suppression of GSK-3beta activity mimicked HGF and abolished RANTES expression, whereas ectopic expression of GSK-3beta restored RANTES induction. HGF also induced renal GSK-3beta phosphorylation and inactivation after obstructive injury in vivo. These observations suggest that HGF is a potent anti-inflammatory cytokine that inhibits renal inflammation by disrupting NF-kappaB signaling and may be a promising therapeutic agent for progressive renal diseases.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blotting, Western
  • Cells, Cultured
  • Chemokine CCL2 / metabolism
  • Chemokine CCL5 / metabolism
  • Chemotaxis, Leukocyte / immunology
  • Enzyme Activation / physiology
  • Enzyme-Linked Immunosorbent Assay
  • Fluorescent Antibody Technique
  • Gene Transfer Techniques
  • Glycogen Synthase Kinase 3 / metabolism
  • Hepatocyte Growth Factor / genetics
  • Hepatocyte Growth Factor / metabolism*
  • Humans
  • I-kappa B Kinase / metabolism
  • Immunohistochemistry
  • Immunoprecipitation
  • Inflammation / metabolism*
  • Kidney Diseases / immunology
  • Kidney Diseases / metabolism*
  • Kidney Diseases / pathology
  • Mice
  • Monocytes / immunology
  • Monocytes / metabolism
  • NF-kappa B / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Rats
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / physiology*
  • T-Lymphocytes / immunology
  • eIF-2 Kinase / metabolism

Substances

  • Chemokine CCL2
  • Chemokine CCL5
  • NF-kappa B
  • Hepatocyte Growth Factor
  • Phosphatidylinositol 3-Kinases
  • eIF-2 Kinase
  • I-kappa B Kinase
  • Glycogen Synthase Kinase 3